Transcriptomic changes triggered by ouabain in rat cerebellum granule cells: Role of α3- and α1-Na+,K+-ATPase-mediated signaling


Autoři: Larisa V. Smolyaninova aff001;  Alexandra A. Shiyan aff001;  Leonid V. Kapilevich aff002;  Alexander V. Lopachev aff003;  Tatiana N. Fedorova aff003;  Tatiana S. Klementieva aff004;  Aleksey A. Moskovtsev aff004;  Aslan A. Kubatiev aff004;  Sergei N. Orlov aff001
Působiště autorů: Department of Biomembranes, Faculty of Biology, M. V. Lomonosov Moscow State University, Moscow, Russia aff001;  Department of Sports Tourism Sports Physiology and Medicine, National Research Tomsk State University, Tomsk, Russia aff002;  Laboratory of Clinical and Experimental Neurochemistry, Research Center of Neurology, Moscow, Russia aff003;  Department of Molecular and Cell Pathophysiology, Institute of General Pathology and Pathophysiology, Moscow, Russia aff004;  Central Research Laboratory, Siberian Medical State University, Tomsk, Russia aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222767

Souhrn

It was shown previously that inhibition of the ubiquitous α1 isoform of Na+,K+-ATPase by ouabain sharply affects gene expression profile via elevation of intracellular [Na+]i/[K+]i ratio. Unlike other cells, neurons are abundant in the α3 isoform of Na+,K+-ATPase, whose affinity in rodents to ouabain is 104-fold higher compared to the α1 isoform. With these sharp differences in mind, we compared transcriptomic changes in rat cerebellum granule cells triggered by inhibition of α1- and α3-Na+,K+-ATPase isoforms. Inhibition of α1- and α3-Na+,K+-ATPase isoforms by 1 mM ouabain resulted in dissipation of transmembrane Na+ and K+ gradients and differential expression of 994 transcripts, whereas selective inhibition of α3-Na+,K+-ATPase isoform by 100 nM ouabain affected expression of 144 transcripts without any impact on the [Na+]i/[K+]i ratio. The list of genes whose expression was affected by 1 mM ouabain by more than 2-fold was abundant in intermediates of intracellular signaling and transcription regulators, including augmented content of Npas4, Fos, Junb, Atf3, and Klf4 mRNAs, whose upregulated expression was demonstrated in neurons subjected to electrical and glutamatergic stimulation. The role [Na+]i/[K+]i-mediated signaling in transcriptomic changes involved in memory formation and storage should be examined further.

Klíčová slova:

DNA-binding proteins – Gene expression – MTT assay – Neurons – Transcriptome analysis – Cerebellum – Olfactory receptors – Granule cells


Zdroje

1. Herrera VL, Emanuel JR, Ruiz-Opazo N, Levenson R, Nadal-Ginard B. Three differentially expressed Na,K-ATPase alpha subunit isoforms: structural and functional implications. J Cell Biol. 1987; 105:1855–1865. doi: 10.1083/jcb.105.4.1855 2822726

2. Sweadner KJ. Isozymes of the Na+/K+-ATPase. Biochim Biophys Acta. 1989; 988:185–220. doi: 10.1016/0304-4157(89)90019-1 2541792

3. Shamraj OI, Lingrel JB. A putative fourth Na,K-ATPase α-subunit is expressed in testis. Proc Natl Acad Sci USA. 1994; 91:12952–12956. doi: 10.1073/pnas.91.26.12952 7809153

4. Blanco G, Sanchez G, Melton RJ, Tourtellotte WG, Mercer RW. The alpha4 isoform of the Na,K-ATPase is expressed in the germ cells of the testes. J Histochem and Cytochem. 2000; 48:1023–1032. doi: 10.1177/002215540004800801 10898797

5. Benarroch EE. Na+,K+-ATPase: functions in the nervous system and involvement in neurologic disease. Neurology. 2011; 76(3):287–293. doi: 10.1212/WNL.0b013e3182074c2f 21242497

6. Blanco G. Na/K-ATPase subunit heterogeneity as a mechanism for tissue specific ion regulation. Semin Nephrol. 2005; 25:292–303. doi: 10.1016/j.semnephrol.2005.03.004 16139684

7. Blanco G, Mercer RW. Isozymes of the Na,K-ATPase: heterogeneity in structure, diversity in function. Am J Physiol. 1998; 275 (5):F633–F650. doi: 10.1152/ajprenal.1998.275.5.F633 9815123

8. Geering K. Function of FXYD Proteins, Regulators of Na,K-ATPase. J Bioenerg Biomembr. 2005; 37(6):387–392. doi: 10.1007/s10863-005-9476-x 16691470

9. Béguin P, Crambert G, Guennoun S, Garty H, Horisberger JD, Geering K. CHIF, a member of the FXYD protein family, is a regulator of Na,K-ATPase distinct from the gamma-subunit. EMBO J. 2001; 20(15):3993–4002. doi: 10.1093/emboj/20.15.3993 11483503

10. Béguin P, Crambert G, Monnet-Tschudi F, Uldry M, Horisberger JD, Garty H, et al. FXYD7 is a brain-specific regulator of Na,K-ATPase alpha 1-beta isozymes. EMBO J. 2002; 21(13):3264–3273. doi: 10.1093/emboj/cdf330 12093728

11. Li C, Crambert G, Thuillard D, Roy S, Schaer D, Geering K. Role of the transmembrane domain of FXYD7 in structural and functional interactions with Na,K-ATPase. J Biol Chem. 2005; 280(52):42738–42743. doi: 10.1074/jbc.M508451200 16269407

12. Arystarkhova E, Wetzel RK, Asinovski NK, Sweadner KJ. The gamma subunit modulates Na(+) and K(+) affinity of the renal Na,K-ATPase. J Biol Chem. 1991; 274(47):33183–33185. doi: 10.1074/jbc.274.47.33183 10559186

13. Pu HX, Cluzeaud F, Goldshleger R, Karlish SJ, Farman N, Blostein R. Functional role and immunocytochemical localization of the gamma a and gamma b forms of the Na,K-ATPase gamma subunit. J Biol Chem. 2001; 276(23):20370–20378. doi: 10.1074/jbc.M010836200 11278761

14. Garty H, Lindzen M, Scanzano R, Aizman R, Füzesi M, Goldshleger R, et al. A functional interaction between CHIF and Na-K-ATPase: implication for regulation by FXYD proteins. Am J Physiol Renal Physiol. 2002; 283(4):F607–F615. doi: 10.1152/ajprenal.00112.2002 12217851

15. Xie Z, Askari A. Na+/K+-ATPase as a signal transducer. Eur J Biochem. 2002; 269:2434–2439. doi: 10.1046/j.1432-1033.2002.02910.x 12027880

16. Aperia A. New roles for an old Na,K-ATPase emerges as an interesting drug target. J Intern Med. 2007; 261:44–52. doi: 10.1111/j.1365-2796.2006.01745.x 17222167

17. Liu J, Xie Z. The sodium pump and cardiotonic steroids-induced signal transduction protein kinases and calcium-signaling microdomain in regulation of transporter traficking. Biochim Biophys Acta. 2010; 1802: 1237–1245. doi: 10.1016/j.bbadis.2010.01.013 20144708

18. Riganti C, Campia I, Kopecka J, Gazzano E, Doublier S, Aldieri E, et al. Pleiotropic effects of cardioactive glycosides. Curr Med Chem. 2011; 18:872–885. doi: 10.2174/092986711794927685 21182478

19. Orlov SN, Klimanova EA, Tverskoi AM, Vladychenskaya EA, Smolyaninova LV, Lopina OD. Na+i,K+i-dependent and -independent signaling triggered by cardiotonic steroids: facts and artifacts. Molecules. 2017; 22(4): E635. doi: 10.3390/molecules22040635 28420099

20. Hieber V, Siegel GJ, Fink DJ, Beaty MV, Mata M. Differential distribution of (Na,K)-ATPase alpha isoforms in the central nervous system. Cell Mol Neurobiol. 1991; 11:253–262. 1851465

21. McGrail KM, Phillips JM, Sweadner KJ. Immunofluorescent localization of three Na,K-ATPase isozymes in the rat central nervous system: both neurons and glia can express more than one Na,K-ATPase. J Neurosci. 1991; 11:381–391. 1846906

22. Peng L, Martin-Vasallo P, Sweadner KJ. Isoforms of Na,K-ATPase alpha and beta subunits in the rat cerebellum and n granule cell cultures. J Neurosci. 1997; 17: 3488–3502. 9133374

23. Akkuratov EE, Lopacheva OM, Kruusmägi M, Lopachev AV, Shah ZA, Boldyrev AA, et al. Functional interaction between Na/K-ATPase and NMDA receptor in cerebellar neurons. Mol Neurobiol. 2015; 52(3):1726–1734. doi: 10.1007/s12035-014-8975-3 25381029

24. Jewell EA, Lingrel JB. Comparison of the substrate dependence properties of the rat Na,K-ATPase alpha 1, alpha 2, and alpha 3 isoforms expressed in HeLa cells. J Biol Chem. 1991; 266:16925–16930. 1653250

25. Munzer JS, Daly SE, Jewell-Motz EA, Lingrel JB, Blostien R. Tissue- and isoform-specific behavior of the Na,K-ATPase. J Biol Chem. 1994; 269:16668–16676. 8206986

26. Zahler R, Zhang Z-T, Manor M, Boron WF. Sodium kinetics of Na,K-ATPase a isoforms in intact transfected HeLa cells. J Gen Physiol. 1997; 110:201–213. doi: 10.1085/jgp.110.2.201 9236212

27. Dobretsov M, Stimers JR. Neuronal function of alpha3 isofrm of the Na/K-ATPase. Front Biosci. 2005; 10:2372–2396. doi: 10.2741/1704 15970502

28. Azarias G, Kruusmägi M, Connor S, Akkuratov EE, Liu XL, Lyons D, et al. A specific and essential role for Na,K-ATPase α3 in neurons co-expressing α1 and α3. J Biol Chem. 2013; 288:2734–2743. doi: 10.1074/jbc.M112.425785 23195960

29. O’Brien WJ, Lingrel JB, Wallick ET. Ouabain binding kinetics of the rat alpha two and alpha three isoforms of the sodium-potassium adenosine triphosphate. Arch Biochem Biophys. 1994; 310:32–39. doi: 10.1006/abbi.1994.1136 8161218

30. Hara Y, Nikamoto A, Kojima T, Matsumoto A, Nakao M. Expression of sodium pump activities in BALB/c 3T3 cells transfected withcDNA encoding alpha 3-subunits of rat brain Na+,K+-ATPase. FEBS Lett. 1988; 238:27–30. doi: 10.1016/0014-5793(88)80218-7 2844596

31. Berrebi-Betrand I, Maixent JM, Christe G, Lelievre LG. Two active Na+/K+-ATPases of high affinity for ouaban in adult rat brain membranes. Biochim Biophys Acta. 1990; 1021:148–156. doi: 10.1016/0005-2736(90)90027-l 2154257

32. Atterwill CK, Cunningham VJ, Balazs R. Characterization of Na+,K+-ATPase in cultured and separated neuronal and glial cells from rat cerebellum. J Neurochem. 1984; 43:8–18. doi: 10.1111/j.1471-4159.1984.tb06672.x 6144733

33. Lopachev AV, Lopacheva OM, Osipova EA, Vladychenskaya EA, Smolyaninova LV, Fedorova TN, et al. Ouabain-induced changes in MAP kinase phosphorylation in primary culture of rat cerebellar cells. Cell Biochem Funct. 2016; 34:367–377. doi: 10.1002/cbf.3199 27338714

34. Levi G, Aloisi F, Ciotti MT, Gallo V. Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating cerebellar granule cell cultures. Brain Res. 1984; 290(1):77–86. doi: 10.1016/0006-8993(84)90737-6 6140986

35. Pearson K. On lines and planes of closest fit to systems of points in space. Philos Mag. 1901; 2: 559–572.

36. Akimova OA, Tverskoi AM, Smolyaninova LV, Mongin AA, Lopina OD, La J. Critical role of the α1-Na+,K+-ATPase subunit in insensitivity of rodent cells to cytotoxic action of ouabain. Apoptosis. 2015; 20:1200–1210. doi: 10.1007/s10495-015-1144-y 26067145

37. de Sá Lima L, Kawamoto EM, Munhoz CD, Kinoshita PF, Orellana AM, Curi R, et al. Ouabain activates NFκB through an NMDA signaling pathway in cultured cerebellar cells. Neuropharmacology. 2013; 73:327–36. doi: 10.1016/j.neuropharm.2013.06.006 23774137

38. Akimova OA, Mongin AA, Hamet P, Orlov SN. The rapid decline of MTT reduction is not a marker of death signaling in ouabain-treated cells. Cell Mol Biol. 2006; 52 (8):71–77. 17535739

39. Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of Gene Ontology terms. PLoS ONE. 2011; 6(7):e21800. doi: 10.1371/journal.pone.0021800 21789182

40. Schlicker A, Domingues FS, Rahnenführer J, Lengauer T. A new measure for functional similarity of gene products based on Gene Ontology. BMC bioinformatics. 2006; 7:302. doi: 10.1186/1471-2105-7-302 16776819

41. Olender T, Lancet D, Nebert DW. Update on the olfactory receptor (OR) gene superfamily. Hum Genomics. 2008; 3:87–97. doi: 10.1186/1479-7364-3-1-87 19129093

42. Lowe G, Nakamura T, Gold GH. Adenylate cyclase mediates olfactory transduction for a wide variety of odorants. Proc Natl Acad Sci USA. 1989; 86:5641–5645. doi: 10.1073/pnas.86.14.5641 2787513

43. Nakamura T, Gold GH. A cyclic nucleotide-gated conductance in olfactory receptor glia. Nature. 1987; 325: 442–444. doi: 10.1038/325442a0 3027574

44. Kohl JV, Altzmueller M, Fink B, Grammer K. Human pheromones: integrating neuroendocrinology and ethology. Neuro Endocrinol Lett. 2001; 22:309–321. 11600881

45. Kang N, Koo J. Olfactory receptors in non-chemosensory tissues. BMB Rep. 2012; 45:612–622. doi: 10.5483/BMBRep.2012.45.11.232 23186999

46. Sidorenko SV, Klimanova E, Milovanova K, Lopina OD, Kapilevich LV, Chibalin AV, et al. Transciptomic changes in C2C12 myotubes triggered by electrical stimulation: role of Ca2+i-mediated and Ca2+i-independent signaling and elevated [Na+]i/[K+]i ratio. Cell Calcium. 2018; 76:72–86. doi: 10.1016/j.ceca.2018.09.007 30300758

47. Dai W, Li W, Hoque M, Li Z, Tian B, Makeyev EV. A post-transcriptional mechanism pacing expression of neural genes with precursor cell differentiation status. Nat Commun. 2015; 6:7576. doi: 10.1038/ncomms8576 26144867

48. Mei Y, Yuan Z, Song B, Li D, Ma C, Hu C, et al. Activating transcription factor 3 up-regulated by c-Jun NH(2)-terminal kinase/c-Jun contributes to apoptosis induced by potassium deprivation in cerebellar granule neurons. Neuroscience. 2008; 151:771–779. doi: 10.1016/j.neuroscience.2007.10.057 18178318

49. Ortega-Martinez S. A new perspective on he role of the CREB family of transcription factors in memory consolidation via adult hipocampus neurogenesis. Front Mol Neurosci. 2015; 8:46. doi: 10.3389/fnmol.2015.00046 26379491

50. Flavell SW, Greenberg ME. Signaling mechanisms linking neuronal activity to gene expressoin and plasticity of the nervous system. Annu Rev Neurosci. 2008; 31:563–590. doi: 10.1146/annurev.neuro.31.060407.125631 18558867

51. Zhu S, Tai C, MacVicar BA, Jia W, Cynader MS. Glutamatergic stimulation triggers rapid Krupple-Like factor 4 expression in neurons and the overexpression of KLF4 sensitizes neurons to NMDA-induced caspase-3 activity. Brain Res. 2009; 1250:49–62. doi: 10.1016/j.brainres.2008.11.013 19041854

52. Poo MM. Neurotrophins as synaptic modulators. Nature Reviews Neuroscience. 2001; 2: 24–32. doi: 10.1038/35049004 11253356

53. Tyler WJ, Alonso M, Bramham CR, Pozzo-Miller LD. From acquisition to consolidation, on the role of brain-derived neurotrophic factor signaling signaling in hippocampal-dependent learning. Learn Mem. 2002; 9:224–237. doi: 10.1101/lm.51202 12359832

54. Lin Y, Bloodgood BL, Hauser JL, Lapan AD, Koon AC, Kim TK, et al. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature. 2008. 455(7217): 1198–1204. doi: 10.1038/nature07319 18815592

55. Gao T, Qian S, Shen S, Zhang X, Liu J, Jia W, et al. Reduction of mitochondrial 3-oxoacyl-ACP synthase (OXSM) by hyperglycemia is associated with deficiency of α-lipoic acid synthetic pathway in kidney of diabetic mice. Biochem Biophys Res Commun. 2019; 512(1):106–111. doi: 10.1016/j.bbrc.2019.02.155 30871779

56. Klimanova EA, Tverskoi AM, Koltsova SV, Sidorenko SV, Lopina OD, Tremblay J, et al. Time- and dose-dependent actions of cardiotonic steroids on transcriptome and intracellular content of Na+ and K+: a comparative analysis. Sci Rep. 2017; 7:45403. doi: 10.1038/srep45403 28345607

57. La J, Reed EB, Koltsova S, Akimova O, Hamanaka RB, Mutlu GM, et al. Regulation of myofibroblast differentiation by cardiac glycosides. Am J Physiol Lung Cell Mol Physiol. 2016; 310:L815–L823. doi: 10.1152/ajplung.00322.2015 26851261

58. Smolyaninova LV, Koltsova SV, Sidorenko SV, Orlov SN. Augemented gene expression triggered by Na+,K+-ATPase inhibition: role of Ca2+-mediated and -independent excitation-transcription coupling. Cell Calcium. 2017; 68:5–13. doi: 10.1016/j.ceca.2017.10.002 29129208

59. Gundersen K. Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev. 2011; 86:564–600. doi: 10.1111/j.1469-185X.2010.00161.x 21040371

60. Orlov SN, Hamet P. Salt and gene expression: evidence for Na+i,K+i-mediated signaling pathways. Pflugers Arch—Eur J Physiol. 2015; 467: 489–498. doi: 10.1007/s00424-014-1650-8 25479826

61. Hardingham GE, Chawla S, Johnson CM, Bading H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature. 1997; 385:260–265. doi: 10.1038/385260a0 9000075

62. Landsberg JW, Yuan XJ. Calcium and TRP channels in pulmonary vascular smooth muscle cell proliferation. News Physiol Sci. 2004; 19:44–50. 15016901

63. Taurin S, Dulin NO, Pchejetski D, Grygorczyk R, Tremblay J, Hamet P, et al. c-Fos expression in ouabain-treated vascular smooth muscle cells from rat aorta: evidence for an intracellular-sodium-mediated, calcium-independent mechanism. J Physiol. 2002; 543:835–847. doi: 10.1113/jphysiol.2002.023259 12231642

64. Koltsova SV, Trushina Y, Haloui M, Akimova OA, Tremblay J, Hamet P, et al. Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca2+i-independent excitation-transcription coupling. PLoS One. 2012; 7(5):e38032. doi: 10.1371/journal.pone.0038032 22666440

65. Koltsova SV, Tremblay J, Hamet P, Orlov SN. Transcriptomic changes in Ca2+-depleted cells: role of elevated intracellular [Na+]/[K+] ratio. Cell Calcium. 2015; 58:317–324. doi: 10.1016/j.ceca.2015.06.009 26183762

66. Greger IH, Watson JF, Cull-Candy SG. Structural and functional architecture of AMPA-type glutamate receptors and their auxiliary proteins. Neuron. 2017; 94:713–730. doi: 10.1016/j.neuron.2017.04.009 28521126

67. Bean BP. The action potentil in mammalian central neurons. Nature Rev Neurosci. 2007; 8: 451–465. doi: 10.1038/nrn2148 17514198

68. Callaway JC, Ross WN. Spatial distribution of synaptically activated sodium concentration changes in cerebellar Purkinje neurons. J Neurophysiol. 1997; 77:145–152. doi: 10.1152/jn.1997.77.1.145 9120555

69. Bennay M, Langer J, Meier SD, Kafitz KW, Rose CR. Sodium signals in cerebellar Purkinje neurons and bergmann glial cells evoked by glutamatergic synaptic transmission. Glia. 2008; 56: 1138–1149. doi: 10.1002/glia.20685 18442095

70. Knopfel T, Guatteo E, Bernardi G, Mercuri NB. Hyperpolarization induces a rise in intracellular sodium concentration in dopamine cells of the substantia nigra pars compacta. Eur J Neurosci. 1998; 10:1926–1929. doi: 10.1046/j.1460-9568.1998.00195.x 9751162

71. Kiedrowski L, Wroblewski JT, Costa E. Intracellular sodium concentration in cultured cerebellar granule cells challenged with glutamate. Mol Pharmacol. 1994. 45:1050–1054. 7910657

72. Linden DJ, Smeyne M, Connor JA. Induction of cerebellar long-term depression in culture requires postsynaptic action of sodium ions. Neuron. 1993; 11:1093–1100. doi: 10.1016/0896-6273(93)90222-d 7506045

73. Schoner W, Scheiner-Bobis G. Endogenous and exogenous cardiac glycosides: their role in hypertension, salt metabolism, and cell growth. Am J Physiol Cell Physiol. 2007; 293:C509–C536. doi: 10.1152/ajpcell.00098.2007 17494630

74. Karpova LV, Bulygina ER, Boldyrev AA. Different neuronal Na(+)/K(+)-ATPase isoforms are involved in diverse signaling pathways. Cell Biochem Funct. 2010; 28(2):135–141. doi: 10.1002/cbf.1632 20087845


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